Elsevier

Cognition

Volume 109, Issue 3, December 2008, Pages 372-388
Cognition

Attentional loads associated with interlimb interactions underlying rhythmic bimanual coordination

https://doi.org/10.1016/j.cognition.2008.10.002Get rights and content

Abstract

Studies of rhythmic bimanual coordination under dual-task conditions revealed (1) a dependence of secondary task performance on the stability of coordinative tasks, in that secondary task performance was better during in-phase than antiphase coordination, and (2) a shift in the mean relative phasing between the limbs compared to single-task conditions. The present study aimed to account for these phenomena by dissociating three qualitatively different interactions between the limbs that govern this motor behavior, related to movement planning, error correction, and interlimb reflex activity. The experiment probed the cognitive demands associated with each interlimb interaction by examining the attentional load under dual-task conditions, indexed by reaction times of the secondary task and kinematic changes in the coordinative tasks relative to single-task conditions. First, only in the condition that involved interlimb interactions at the level of movement planning reaction times were shorter for in-phase than for antiphase coordination, highlighting an intimate relation between movement planning and attentional processes. Second, under dual-task conditions a shift in the mean relative phase was observed relative to single-task conditions, but only for the interlimb interactions that depend directly on sensory feedback (error correction and interlimb reflex activity). These observations qualified the effects of attentional load reported in previous studies. Third, reaction times varied systematically over the movement cycle. These variations revealed a dynamical signature of the attentional load that differed between the three interlimb interactions.

Introduction

Coordinated rhythmic movements are ubiquitous in daily life and occur during largely automated actions like walking and breathing but also during activities that require much more skill and training, like piano playing or dancing. Although most of us can readily picture ourselves talking to a friend while strolling through a park, similar dual-tasking is not readily afforded while being engaged in, for example, performing one of Chopin’s nocturnes. In other words, the attentional demands imposed by rhythmic interlimb coordination vary greatly with the degree of difficulty and consequently certain types of coordination impose much larger demands on our cognitive capacities than others. The present study addresses this issue experimentally by examining a classical motor control task of intermediate difficulty, in which both hands move rhythmically with the same tempo in one of two bimanual patterns. This intermediate difficulty is the result of three factors: (1) the specific bimanual pattern to be performed, (2) the elimination of visual feedback of the hand movements, and (3) explicit prescription of movement tempo. Under these circumstances attentional demands are substantial, but not so severe that dual-tasking is no longer possible.

Both qualitatively and computationally motor control can be regarded as similar to social interaction, in the sense that it involves input-output relations governed by predictions and expectations based on experience, and as such may even serve as a template for a theory of mind (Wolpert, Doya, & Kawato, 2003). This is an important (although perhaps slightly exaggerated) point as it clearly breaks with ideas that are rooted in mind-body dualism, which refer to motor control in terms of “low-level” sensorimotor representations as opposed to “high-level” cognitive processes such as perception, memory, and language comprehension, and arguably have led to a neglect of motor control in the science of mental life and behavior (Rosenbaum, 2005). In contrast, motor control constitutes a form of cognition in the sense that every coordinated action requires the planning of well-orchestrated activity patterns and associated correction processes verifying the outcome (Grush, 2004, Wolpert and Ghahramani, 2000). These activities, which are cognitive in nature, should not be confused with (or reduced to) “low-level” aspects like musculoskeletal dynamics itself or the specialized neural circuitry underlying reflexes. Conversely, in the literature on situated (or embodied, cf. Barsalou, 2008) cognition, it has become evident that cognitive activity takes place in the context of a real body and a real environment (Clark, 1997), and is thus intrinsically linked to perceptual and motor processes, even when it is decoupled from the environment and the on-line performance of specific actions (for reviews, see, e.g., Barsalou, 2008, Wilson, 2002). From this conceptual background we sought to unravel the interface between attentional processes and the interlimb interactions underlying bimanual coordination to be presented below. As the interactions in question reside at different functional levels of the motor hierarchy, we anticipated that different attentional loads would be associated with each source of interlimb interaction. By specifically examining these attentional loads we aimed to detail, and expand on, previous findings on the relation between attentional processes and bimanual coordination.

In general, bimanual coordination of isofrequency movements (i.e., both hands moving with the same frequency) is a classical motor task of moderate difficulty that has been studied extensively. Hence, its behavioral characteristics are well-known. First, because both hands are engaged in identical, equally simple subtasks and move at the same frequency, the bimanual movement pattern is unequivocally quantifiable in terms of the relative phase (Φ) between the hands (e.g., Haken et al., 1985, Kelso, 1984). Second, it is readily appreciated that despite the simplicity of the subtasks severe constraints are involved in bimanual isofrequency coordination (Carson and Kelso, 2004, Swinnen, 2002), which are a consequence of the interactions between the limbs. This is evidenced by the limited number of coordination patterns (i.e., two) that can be performed in a stable, reliable fashion without training (Zanone & Kelso, 1992). These patterns are commonly referred to as in-phase (Φ = 0°) and antiphase (Φ = 180°) coordination. In the context of the present study, in-phase coordination refers to both hands moving in a mirror-symmetric fashion (involving simultaneous activation of homologous muscles), whereas antiphase coordination refers to both hands moving in the same direction (involving alternating activation of homologous muscles). Third, in-phase coordination is easier to perform than antiphase coordination and at higher frequencies the antiphase pattern becomes unstable, resulting in involuntary transitions to the (still stable) in-phase pattern (Haken et al., 1985, Kelso, 1984). Because these behavioral characteristics are quite specific (viz., a small number of easily quantifiable bimanual patterns with different stability characteristics) and open to empirical evaluation, this task provides an ideal context for experimental studies on the interlimb interactions that govern rhythmic bimanual coordination.

In the past two decades, theoretical accounts of the behavioral phenomena in rhythmic bimanual coordination have emphasized contributions of three different sources of interlimb interaction to this coordinative stability, pertaining to different aspects of motor control. First, interlimb interactions related to movement planning and open-loop control have been assigned a prominent role, based on both empirical (Helmuth and Ivry, 1996, Ridderikhoff et al., 2005, Spencer et al., 2005) and theoretical (Grossberg, Pribe, & Cohen, 1997) considerations. In general, open-loop control reflects a type of control in which the input to the musculoskeletal system does not depend on sensory feedback about the ongoing movements, in contrast to closed-loop control in which sensory feedback signals are used to adapt these inputs, for example to counteract unexpected perturbations. Because of this characteristic, open-loop control is anticipatory and closely associated with movement planning.

The other two sources of interlimb interaction refer to aspects of closed-loop control. The second source of interlimb interaction highlights a role for error corrections based on sensory feedback of the ongoing movements (e.g., Baldissera et al., 1991, Carson and Riek, 1998b, Cohen, 1971, Ridderikhoff et al., 2007), and more recently the potent role of perceptual information in stabilizing rhythmic bimanual patterns (e.g., Mechsner et al., 2001, Wilson et al., 2003). This is a high-level (adaptable) form of closed-loop control in the sense that the sensory feedback is evaluated with reference to the task at hand. In contrast, the third source of interlimb interaction is a relatively automatic (or reflex-like) mechanism based on peripheral reflexes. Such a mechanism has been proposed to underlie phase entrainment in rhythmic bimanual coordination (Baldissera et al., 1991, Carson and Riek, 1998b, Ridderikhoff et al., 2006) and interlimb coordination during animal locomotion (for a review, see Duysens, Clarac, & Cruse, 2000). In general, phase entrainment1 refers to the effect that the timing of the movements of one limb is influenced by the movement of the other resulting in an attraction to a specific relative timing, or relative phase, between the limbs.

Against this background, we recently devised a method to evaluate the contributions of these three distinct sources of interlimb interaction in conjunction (Ridderikhoff et al., 2005). To reiterate, these interlimb interactions are deduced from the existing literature on rhythmic bimanual coordination and associated with movement planning, error correction and reflex-like behavior, respectively. In practice, our method is based on an operational definition of these sources of interlimb interaction that distinguishes them in two regards: intentionality and sensory dependence. Since bimanual coordination is intended a priori in planning and correction interactions, these two sources of interlimb interactions are associated with the intention to perform a bimanual coordination pattern, in contrast to reflex interactions which are induced automatically by sensory signals from the opposite (or contralateral) limb. Furthermore, two sources of interaction (correction and reflex interactions) depend on sensory signals, while planning interactions do not, which is another way to phrase the aforementioned distinction between closed-loop and open-loop processes.

Based on these operational definitions (see Table 1), our experimental method consisted of four different tasks in which these interlimb interactions are implicated in different degrees. Two unimanual tasks were examined for reference (UN: no interaction) and to delineate the unintentional reflex entrainment (UNm: interaction induced by passive movement of the opposite hand). Two bimanual tasks allowed for an assessment of the relative contributions of error corrections, which are involved in the kinesthetic tracking of a passive movement (KT), and planning, which contributes only to the stability of active bimanual coordination (AB: both hands actively moving). Details regarding these tasks as well as their mapping onto the sources of interlimb interaction (cf. Table 2) are provided in Section 2. Most importantly, the comparison between these four tasks enabled us to assess the contributions of each source of interlimb interaction to the coordinative stability (cf. Ridderikhoff et al., 2005).

The proposed sources of interlimb interaction can be defined in terms of, for example, the associated behavioral effects, the underlying neural substrate, or the defining functional characteristics. We previously adopted an approach in which we framed them in terms of the associated behavioral effects and related our observations to the literature to garner a speculative account of the neural substrate of these interactions (Ridderikhoff et al., 2005). However, an emphasis on the functional characteristics of these interactions (viz. movement planning, error correction, and interlimb reflex activity) was appropriate in the context of the present study. To preserve the continuity of our studies the associated behavioral effects are also included in Table 1. Although the short-hand terms (planning, correction, and reflex) provided a convenient – concise and apt – terminology, the reader is reminded that in the present paper these terms reflect only aspects of interactions underlying rhythmic interlimb coordination. We do not claim that the obtained results can be generalized to other forms of movement planning, error corrections, and reflex activity.

The present study extended our previous work by examining the attentional load associated with these sources of interlimb interaction using a dual-task setup, in which the four coordinative tasks were performed both in isolation and while performing a secondary reaction time (RT) task. If the coordinative tasks are prioritized, the secondary task can be used to probe the attentional resources required to perform the four aforementioned tasks (cf., e.g., Summers, Maeder, Hiraga, & Alexander, 2008), with the RTs serving as an index of the attentional load (larger RTs indicating higher attentional demands of the coordinative task). According to our method comparisons between these tasks provided a selective focus on the attentional resources associated with the interlimb interactions involved (see Table 2). This analysis served two purposes. First, it provided a global indication of the central cost associated with each interaction, which may depend on the coordination pattern (in-phase or antiphase). Second, more local changes in the attentional demands during the cycle (if any) may be informative about the dynamics of the interlimb interactions involved. Such local changes in RTs have been observed before during unimanual rhythmic tracking movements (Michaels & Bongers, 1994). Whereas the analysis of local changes in the attentional demands during the cycle will be exploratory in nature, two explicit hypotheses were formulated concerning the attentional loads associated with the three sources of interlimb interaction, as outlined in the following.

Several studies have examined the attentional demands of rhythmic bimanual coordination using dual-task experiments. In single-task experiments it has been demonstrated that directing the attentional focus (e.g., to a specific hand or to spatial or temporal aspects of the performance) affects the coordinative stability of the task (Hiraga et al., 2005, Wuyts et al., 1996). Furthermore, using a secondary reaction time task, a relationship between pattern stability and performance on the secondary task (higher stability corresponds to better secondary task performance) has been observed in experiments involving neuromuscular effects on unimanual synchronization (Carson, Chua, Byblow, Poon, & Smethurst, 1999), and rhythmic bimanual coordination (Monno et al., 2000, Monno et al., 2002, Summers et al., 1998, Summers et al., 2008, Temprado et al., 1999, Temprado et al., 2001, Zanone et al., 2001).

This relationship between the stability of the coordination task and the performance on a secondary task was not observed, however, when other secondary tasks were used (counting backwards in threes: Pellecchia et al., 2005, Pellecchia and Turvey, 2001; encoding and retrieval of words: Shockley and Turvey, 2005, Shockley and Turvey, 2006). In contrast, in the latter four studies marked additional shifts in the mean relative phase between the hands were observed under dual-task conditions. In this respect, it is of interest to note that in these studies the coordinative stability was manipulated mainly through detuning (or asymmetric loading) of the limbs during in-phase coordination, rather than by comparison of in-phase and antiphase coordination (antiphase coordination was studied, but no effects were found, in Pellecchia & Turvey, 2001). In short, detuning describes systematic changes in the mean relative phase and its variability as a result of unequal loading of the limbs (e.g., by means of using two pendulums with different natural frequencies). In general, the limb with the lower natural frequency (e.g., higher inertia) lags the other limb, resulting in a shift of the mean relative phase. In these studies (Pellecchia and Turvey, 2001, Pellecchia et al., 2005, Shockley and Turvey, 2005, Shockley and Turvey, 2006), enhanced effects of detuning on the mean relative phase were observed under dual-task conditions.

Because rhythmic bimanual coordination is the result of interactions between the limbs, the present study investigated whether the discrepancy between these findings can be accounted for by assuming that different interlimb interactions underlie (1) the stabilization of bimanual coordination patterns, and (2) the shift in the mean relative phase (viz. interactions that are affected by detuning).

To examine the attentional load associated with each source of interlimb interaction, priority was assigned to the coordinative tasks (viz. AB, KT, UNm, and UN – see Section 1.2) during dual-task performance and reaction times (RT) on a secondary task were used as an index of the attentional demands of the coordinative task. This prioritization of the coordinative task was expected to limit the differences in coordinative stability between single-task and dual-task conditions (cf. Temprado et al., 1999). Two explicit hypotheses were formulated. First, our previous work (using a similar methodology) indicated on the basis of kinematical and electromyographical analyses that the movement planning underlying the open-loop control of the bimanual patterns is the main contributor to the (differential) stability of in-phase and antiphase coordination (Ridderikhoff et al., 2005). This led to the hypothesis that this source of interaction underwrites the general relation between pattern stability and attentional cost. Thus, planning-related interactions were predicted to yield larger RTs for antiphase than for in-phase coordination. Second, because detuning is induced by changing the inertial properties of the limbs, such peripheral changes affect the relation between the open-loop control signal and the actual movement patterns (Peper et al., 2004, Ridderikhoff et al., 2004). Such changes are most likely engendered by interlimb interactions that depend on sensory signals (correction and reflex interactions). We therefore hypothesized that, in dual-task conditions, shifts in the mean relative phase would occur for the interactions related to error correction and interlimb reflex activity, but not for the interactions related to planning.

Section snippets

Methods

Eight participants (mean age 24.8 yr, SD 2.1 yr) were included in the experiment. Six were right-handed and two were left-handed as determined by an inventory (Oldfield, 1971). None of them had known neurological impairments and all had normal or corrected to normal vision. The experiment was approved by the ethics committee of the Faculty of Human Movement Sciences of VU University Amsterdam. All participants gave their informed consent prior to participation.

Results

Nonstationarity of the kinematics and technical problems resulted in the exclusion of 18 and 59 of the 752 trials, respectively. All RTs in the excluded trials and all other RTs that were classified as outliers were discarded (in total 433 responses out of 2880). The distribution of these excluded trials and responses revealed no marked variations over conditions. In the following, the results are presented as population mean ± the standard (between-subjects) error of the mean. The results

Discussion

In the Introduction we already emphasized that motor control involves cognitive processes related to planning and error correction respectively, and that these cognitive aspects give rise to two distinct sources of interlimb interaction. Before discussing the present results in detail, it is useful to make some further theoretical remarks on the relations between movement, cognition and dual-tasking. In the literature several theories exist that are built on the idea that the cognitive system

Conclusion

In the present study we applied a previously developed and established methodology (Ridderikhoff et al., 2005) in combination with a dual-task protocol to assess the attentional load associated with three sources of interlimb interaction underlying rhythmic bimanual coordination. In addition to the outcome of the single-task performance of the coordinative tasks, which corroborated our previous findings, the dual-task conditions provided grounds for original interpretations of two findings that

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